Adult deafness induces somatosensory conversion of ferret auditory cortex

Abstract

In response to early or developmental lesions, responsiveness of sensory cortex can be converted from the deprived modality to that of the remaining sensory systems. However, little is known about capacity of the adult cortex for cross-modal reorganization. The present study examined the auditory cortices of animals deafened as adults, and observed an extensive somatosensory conversion within as little as 16 days after deafening. These results demonstrate that cortical cross-modal reorganization can occur after the period of sensory system maturation.aging ͉ cross-modal reorganization ͉ hearing loss ͉ plasticity ͉ reorganization T he study of neural plasticity has revealed the considerable vulnerability of the developing brain to altered sensory experience (1). This vulnerability is particularly evident when the loss of peripheral sensory input results in the cross-modal reorganization of cortex. In their classic study, Rauschecker and Korte (2) showed that the ectosylvian visual area responded vigorously to auditory and/or somatosensory stimuli in cats visually deprived from birth. Similar developmental studies have been performed in a variety of species and their common finding was that cortical areas normally devoted to processing one sensory modality were converted to the other sensory systems following early visual deprivation (3-8) or early deafening (9-13, but see 14).In contrast to these established developmental effects, little is known about the potential for cross-modal reorganization from lesions occurring after the sensory systems have matured. The few animal studies of adult cross-modal reorganization have described far less robust effects and collectively appear inconclusive. Blinding of adult rabbits resulted in somatosensory innervation of primary visual cortex near its border with somatosensory cortex (15). However, in deafened auditory cortex (16), visual responses were observed in the primary auditory area of cats deafened at 1 week of age, but not when cats were deafened at a later stage. In humans, regions of multi-sensory cortex become more visually active after late-onset deafness (17), which is not surprising given the presence of visual inputs before the hearing loss.Despite these limited and equivocal results regarding lateonset cross-modal reorganization, there is considerable evidence that the adult cortex is capable of reacting to loss of peripheral input (18,19). Investigations of adult subjects that received peripheral insults such as digit amputation (20), focal retinal lesions (21, 22), and frequency-specific cochlear lesions (23) revealed that the initially silenced cortical locus eventually developed responses similar to those of unaffected neighboring neurons (18,24). Although these effects occurred within the same modality, the fact that intra-modal reorganization had occurred is consistent with the likelihood that the sensory cortices of adults are indeed mutable.Hearing impairment is one of the most prevalent neurological disorders in humans, affecting 16% of adults in the...

Bimodal stimulus timing-dependent plasticity in primary auditory cortex is altered after noise exposure with and without tinnitus

“…These findings are consistent with the neural modulation and changes in bimodal plasticity in DCN following noise exposure and tinnitus and suggest that mechanisms of auditory-somatosensory integration at the brain stem have influence across the central auditory circuit in tinnitus (Koehler and Shore 2013b). This is important to consider given the known extensive cross-modal reorganization of the auditory cortex following noise exposure in which 84% of sampled auditory cortex neurons began to respond to somatosensory stimulation with 76 dB or greater threshold shifts (Allman et al 2009). The authors of the latter paper acknowledge that their findings may be due, at least in part, to deafness-induced increases in somatosensory inputs to the DCN (Shore et al 2008;Zeng et al 2012), the first station of the central auditory relay, which may generate upstream changes seen at the cortical level.…”

“…While it is evident that somatosensory stimulation can modulate auditory responses in A1 (Allman et al 2009;Basura et al 2012;Ghazanfar et al 2005Ghazanfar et al , 2008Lakatos et al 2007;Schroeder and Foxe 2002;Schroeder et al 2001Schroeder et al , 2003, it is not known if these effects are stimulus timing dependent or if they adhere to similar timing rule changes, reflecting STDP as in DCN following noise exposure and tinnitus (Koehler and Shore 2013a,b). …”

Crossmodal reorganization in the early deaf switches sensory, but not behavioral roles of auditory cortex

“…However, it does not appear that the crossmodal inputs to FAES are present at the developmental stages in which deafness was induced (26,34). In addition, given that early deafness induced crossmodal plasticity in 89% of FAES neurons (this study) whereas late deafness generated similar levels in adult A1/anterior auditory field (AAF) (87%) (35), the role of age in deafness-induced crossmodal plasticity remains to be determined. Whether the alternative mechanism involving rewiring also participates in these crossmodal phenomena will require directed connectional studies of deaf animals.…”

Cortical cross-modal plasticity following deafness measured using functional near-infrared spectroscopy

“…This has been used to explain fMRI responses to somatosensory stimulation in auditory brain regions of deaf individuals (Auer et al, 2007). An electrophysiological study has also reported larger cortical responses to vibrotactile stimulation in deaf, compared with normally-hearing ferrets (Allman et al, 2009). Despite the majority of the profoundly-deaf participants in our study (26 out of 30) reporting occasional or regular hearing aid use, contrary to our hypothesis, fNIRS responses in the ROI to somatosensory stimulation were similar between profoundly-deaf and normallyhearing groups.…”